Costs Of Mating Research Articles

Bet-hedging as a mechanism for the evolution of polyandry, revisited.

Females that mate with multiple males (polyandry) may reduce the risk that their eggs are fertilized by a single unsuitable male. About 25 years ago it was hypothesized that bet-hedging could function as a mechanism favoring the evolution of polyandry, but this idea is controversial because theory indicates that bet-hedging via polyandry can compensate the costs of mating only in small populations. Nevertheless, populations are often spatially structured, and even in the absence of spatial structure, mate-choice opportunity can be limited to a few potential partners. We examined the effectiveness of bet-hedging in such situations with simulations carried out under two scenarios: (1) intrinsic male quality, with offspring survival determined by male phenotype (male's ability to generate viable offspring), and (2) genetic incompatibility (offspring fitness determined nonadditively by parental genotypes). We find higher fixation probabilities for a polyandrous strategy compared to a monandrous strategy if complete reproductive failure due to male effects or parental incompatibility is pervasive in the population. Our results also indicate that bet-hedging polyandry can delay the extinction of small demes. Our results underscore the potential for bet-hedging to provide benefits to polyandrous females and have valuable implications for conservation biology.

Polyandrous females provide sons with more competitive sperm: Support for the sexy-sperm hypothesis in the rattlebox moth (Utetheisa ornatrix).

Given the costs of multiple mating, why has female polyandry evolved? Utetheisa ornatrix moths are well suited for studying multiple mating in females because females are highly polyandrous over their life span, with each male mate transferring a substantial spermatophore with both genetic and nongenetic material. The accumulation of resources might explain the prevalence of polyandry in this species, but another, not mutually exclusive, possibility is that females mate multiply to increase the probability that their sons will inherit more-competitive sperm. This latter "sexy-sperm" hypothesis posits that female multiple mating and male sperm competitiveness coevolve via a Fisherian runaway process. We tested the sexy-sperm hypothesis by using competitive double matings to compare the sperm competition success of sons of polyandrous versus monandrous females. In accordance with sexy-sperm theory, we found that in 511 offspring across 17 families, the male whose polyandrous mother mated once with each of three different males sired significantly more of all total offspring (81%) than did the male whose monandrous mother was mated thrice to a single male. Interestingly, sons of polyandrous mothers had a significantly biased sex ratio of their brood toward sons, also in support of the hypothesis.

Complex mitonuclear interactions and metabolic costs of mating in male seed beetles.

The lack of evolutionary response to selection on mitochondrial genes through males predicts the evolution of nuclear genetic influence on male-specific mitochondrial function, for example by gene duplication and evolution of sex-specific expression of paralogs involved in metabolic pathways. Intergenomic epistasis may therefore be a prevalent feature of the genetic architecture of male-specific organismal function. Here, we assess the role of mitonuclear genetic variation for male metabolic phenotypes [metabolic rate and respiratory quotient (RQ)] associated with ejaculate renewal, in the seed beetle Callosobruchus maculatus, by assaying lines with crossed combinations of distinct mitochondrial haplotypes and nuclear lineages. We found a significant increase in metabolic rate following mating relative to virgin males. Moreover, processes associated with ejaculate renewal showed variation in metabolic rate that was affected by mitonuclear interactions. Mitochondrial haplotype influenced mating-related changes in RQ, but this pattern varied over time. Mitonuclear genotype and the energy spent during ejaculate production affected the weight of the ejaculate, but the strength of this effect varied across mitochondrial haplotypes showing that the genetic architecture of male-specific reproductive function is complex. Our findings unveil hitherto underappreciated metabolic costs of mating and ejaculate renewal, and provide the first empirical demonstration of mitonuclear epistasis on male reproductive metabolic processes.

Live fast die young life history in females: evolutionary trade-off between early life mating and lifespan in female Drosophila melanogaster.

The trade-off between survival and reproduction is fundamental to life history theory. Sexual selection is expected to favour a ‘live fast die young’ life history pattern in males due to increased risk of extrinsic mortality associated with obtaining mates. Sexual conflict may also drive a genetic trade-off between reproduction and lifespan in females. We found significant additive genetic variance in longevity independent of lifetime mating frequency, and in early life mating frequency. There was significant negative genetic covariance between these traits indicating that females from families characterized by high levels of multiple mating early in life die sooner than females that engage in less intense early life mating. Thus, despite heritable variation in both traits, their independent evolution is constrained by an evolutionary trade-off. Our findings indicate that, in addition to the well-known male-driven direct costs of mating on female lifespan (mediated by male harassment and harmful effects of seminal fluids), females with a genetic propensity to mate multiply live shorter lives. We discuss the potential role of sexual conflict in driving the evolutionary trade-off between reproduction and lifespan in Drosophila. More generally, our data show that, like males, females can exhibit a live fast die young life history strategy.

Development time of male and female rotifers with sexual size dimorphism

Dwarfism in males is a common phenomenon in planktonic monogonont rotifers. Considering the small body size of males, some studies suggested that the development time of male rotifers is faster than that of females. However, empirical studies associated with such a speculation are scarce. In this study, we used two common rotifer species, Brachionuscalyciflorus and Brachionusplicatilis (each with two geographical populations), to test the hypothesis that the development time of dwarf males is significantly shorter than that of females. Results showed that male eggs (embryos) were deposited much faster than female eggs (embryos) in both Brachionus species. However, the embryonic development time of these small male eggs (embryos) was longer than that of large female eggs (embryos). As a result, males needed significantly longer total development time than females. The total development time of males was 2–3 h longer than that of females in both Brachionus species. Male-producing and female-producing females in the two Brachionus species did not show any difference in development time. Because sexual reproduction begins at high population densities in both species, postponement of development in males will be advantageous by decreasing mating costs in male rotifers.

Developmental environment mediates male seminal protein investment in Drosophila melanogaster.

Summary Males of many species fine‐tune their ejaculates in response to sperm competition risk. Resource availability and the number of competitors during development can also strongly influence sperm production. However, despite the key role of seminal proteins in mediating reproductive processes, it is unclear whether seminal protein investment is dependent on the developmental environment.We manipulated the developmental environment of Drosophila melanogaster by rearing flies at low and high density. As expected, this resulted in large and small (i.e. high and low condition) adult phenotypes, respectively.As predicted, large males produced more of two key seminal proteins, sex peptide (SP) and ovulin, and were more successful at obtaining matings with both virgin and previously mated females. However, there was only a weak and non‐significant trend for large males to transfer more absolute quantities of SP at mating, and thus, small males ejaculated proportionally more of their stored accessory gland SP resources.Males transferred more receptivity‐inhibiting SP to large females. Despite this, large females remated more quickly than small females and thus responded to their developmental environment over and above the quantity of SP they received.The results are consistent with two non‐mutually exclusive hypotheses. First, flies might respond to condition‐dependent reproductive opportunities, with (i) small males investing heavily in ejaculates when mating opportunities arise and large males strategically partitioning SP resources and (ii) small females remating at reduced rates because they have higher mating costs or need to replenish sperm less often.Second, flies may be primed by their larval environment to deal with similar adult population densities, with (i) males perceiving high density as signalling increased competition, leading small males to invest proportionally more SP resources at mating and (ii) females perceiving high density as signalling abundant potential mates, leading to a higher sexual receptivity threshold.Thus, by influencing the mating frequencies of both sexes, as well as the quantity of seminal proteins produced by males and received by females, the developmental environment is likely to have far‐reaching and sex‐specific consequences for sexual selection and sexual conflict.

Live fast, die old: no evidence of reproductive senescence or costs of mating in a damselfly (Odonata: Zygoptera).

Recent examples of actuarial senescence in wild insect populations have challenged the long-held assumption that the brevity of wild insect life spans precludes senescence. We investigate age-related patterns in mating behaviour in adults of a short-lived damselfly, Coenagrion puella and the implications of this mating. Using capture histories for 1033 individuals over two field seasons, we conduct both pooled and stratified analyses of variations in breeding activity. Pooled analyses suggest that there is strong age-related variation in the probability of being present at the mating rendezvous. However, no age-related variation was observed in the probability of mating. Stratified approaches confirmed a general pattern of age-related declines in survival probability, but provided only equivocal evidence of an effect of age on transition between temporary breeding states. Mating males and females showed greater survival than non-mating individuals, possibly as a consequence of higher body condition. Older males that were not currently breeding were less likely to commence breeding on the next day, but showed no patterns in breeding cessation. Overall, transitions between both breeding states declined with age, suggesting that males that breed tend to continue breeding while those that do not breed continue to be unsuccessful. Female mating rates were consistently high across all ages with no age-related decline apparent. While previous research has demonstrated actuarial senescence in this population, as does this study, we find little evidence of either age-related declines in reproductive behaviour or breeding-related declines in survival, which might indicate functional senescence or costs of mating, respectively. Indeed, the greater survival in mating individuals of both sexes suggests that variations in individual quality may mediate both reproductive success and longevity. Contrary to recent studies, we found no compelling evidence for reproductive senescence or a cost of mating in an important and well-studied model odonate. The possible link between condition and ageing suggests that individual quality needs to be taken into account when studying senescence. We recommend the use of multistrata models for the future investigation of these phenomena.

Last male sperm precedence in a polygamous squid

Differential sperm usage from consecutive matings, or sperm precedence, is vital in determining male reproductive success and the outcome of sperm competition for many organisms. Sperm precedence also has significant consequences for mating system dynamics, including both male and female adaptations for increasing reproductive success and avoiding the costs of mating. Despite sexual selection being a strong driver of reproductive behaviour and morphology in cephalopods, surprisingly few studies have investigated sperm dynamics in this group. To redress this gap, we experimentally quantified sperm precedence patterns in the dumpling squid, Euprymna tasmanica, controlling for recent male mating history (first vs. second mating), mating position, and mating frequency. We found that the last male to mate gains an advantage in this system, with the second mating male siring up to 75% of offspring at the beginning of the laying period. The proportion of offspring attributable to the second mating male decreases to 54% by the end of the laying period, potentially as a result of changes in the velocity or number of sperm released from spermatangia over time. There is also significant variation among females in patterns of sperm precedence. This variation was not associated with whether it was the male's first or second mating, male mass, the duration of copulation or the number of pumps (sperm removal behaviour) by the second male. If widespread in cephalopods, last male sperm precedence could help to explain the evolution of mate guarding (or long copulation duration) and sperm removal behaviour in this group.

A captive breeding experiment reveals no evidence of reproductive isolation among lineages of a polytypic poison frog

Reproductive isolation is central to the generation of biodiversity, yet a clear understanding of the contributions of alternative reproductive barriers to this process remains elusive. Studies of young lineages that have diverged in ecologically important traits can offer insights into the chronology and relative importance of various isolating mechanisms during speciation. In poison frogs (Dendrobatidae), within-species lineages often differ dramatically in coloration, a trait subject to natural and sexual selection. Coloration in the strawberry poison frog (Oophaga pumilio) is particularly diverse and previous work suggests the potential for reproductive isolation. We used a captive breeding experiment to assess the extent of reproductive isolation among three allopatric, genetically distinct O. pumilio lineages that differ in coloration. We compared reproduction of within- and between-lineage pairs, predicting that if lineages are isolated, within-lineage pairs would be most successful. We also examined the fertility and productivity of F1 backcrosses of admixed offspring. We found no evidence suggesting behavioural pre-zygotic or post-zygotic reproductive isolation, indicating that isolation would not be maintained by intrinsic mechanisms in the event of secondary contact. Future work should address costs of between-lineage matings exerted by extrinsic natural and/or sexual selection against admixed offspring.

Copulatory wounding and traumatic insemination.

Copulatory wounding (CW) is widespread in the animal kingdom, but likely underreported because of its cryptic nature. We use four case studies (Drosophila flies, Siphopteron slugs, Cimex bugs, and Callosobruchus beetles) to show that CW entails physiological and life-history costs, but can evolve into a routine mating strategy that, in some species, involves insemination through the wound. Although interspecific variation in CW is documented, few data exist on intraspecific and none on individual differences. Although defensive mechanisms evolve in the wound recipient, our review also indicates that mating costs in species with CW are slightly higher than in other species. Whether such costs are dose- or frequency-dependent, and whether defense occurs as resistance or tolerance, decisively affects the evolutionary outcome. In addition to sexual conflict, CW may also become a model system for reproductive isolation. In this context, we put forward a number of predictions, including (1) occasional CW is more costly than routine CW, (2) CW is more costly in between- than within-population matings, and (3) in the presence of CW, selection may favor the transmission of sexually transmitted diseases if they induce resource allocation. Finally, we outline, and briefly discuss, several medical implications of CW in humans.

Effects of noise on sound localization in male grasshoppers, Chorthippus biguttulus

The localization of acoustic signals is an important component of mating behaviour in many species. However, in natural environments sound localization may be hindered by background noise that masks acoustic cues that enable the determination of sound direction by the auditory system. I studied the effects of noise on the sound localization abilities of male grasshoppers, Chorthippus biguttulus, in response to female songs. Males respond to female songs with a stereotyped lateralization behaviour in which they turn towards the perceived sound direction; repetition of this behaviour allows them to approach females. Under quiet conditions, males are highly sensitive to small differences in the timing or amplitude of signals that arrive at each ear. I tested whether noise affected male lateralization accuracy by presenting males with female songs that differed in time or amplitude cues of sound direction, under different levels of masking noise. Noise sharply reduced the responsiveness of males to female songs. However, when males did lateralize the female song, they were surprisingly accurate, even at the highest noise levels. These results suggest that noise only weakly impairs males' directional hearing abilities, but strongly affects their abilities to detect and respond to female songs. Noise therefore probably increases mating costs, because both males and females must expend additional time and energy in mate attraction.

Males Benefit from Mating with Outbred Females in Drosophila littoralis: Male Choice for Female Genetic Quality?

AbstractThe evolution and expression of mate choice behaviour in either sex depends on the sex‐specific combination of mating costs, benefits of choice and constraints on choice. If the benefits of choice are larger for one sex, we would expect that sex to be choosier, assuming that the mating costs and constraints on choice are equal between sexes. Because deliberate inbreeding is a powerful genetic method for experimental manipulation of the quality of study organisms, we tested the effects of both male and female inbreeding on egg and offspring production in Drosophila littoralis. Female inbreeding significantly reduced offspring production (mostly due to lower egg‐to‐adult viability), whereas male inbreeding did not affect offspring production (despite a slight effect of paternal inbreeding on egg‐to‐adult viability). As inbreeding depressed female quality more than male quality, the benefits of mate choice were larger for males than for females. In mate choice experiments, inbreeding did not affect male mating success (measured as a probability to be accepted as a mate in a large group), suggesting that females did not discriminate among inbred and outbred males. In contrast, female mating success was affected by inbreeding, with outbred females having higher mating success than inbred females. This result was not explained by lower activity of inbred females. Our results show that D. littoralis males benefit from mating with outbred females of high genetic quality and suggest adaptive male mate choice for female genetic quality in this species. Thus, patterns of mating success in mate choice trials mirrored the benefits of choice: the sex that benefited more from choice (i.e. males) was more choosy.

Optimal numbers of matings: the conditional balance between benefits and costs of mating for females of a nuptial gift‐giving spider

In species where females gain a nutritious nuptial gift during mating, the balance between benefits and costs of mating may depend on access to food. This means that there is not one optimal number of matings for the female but a range of optimal mating numbers. With increasing food availability, the optimal number of matings for a female should vary from the number necessary only for fertilization of her eggs to the number needed also for producing these eggs. In three experimental series, the average number of matings for females of the nuptial gift-giving spider Pisaura mirabilis before egg sac construction varied from 2 to 16 with food-limited females generally accepting more matings than well-fed females. Minimal level of optimal mating number for females at satiation feeding conditions was predicted to be 2-3; in an experimental test, the median number was 2 (range 0-4). Multiple mating gave benefits in terms of increased fecundity and increased egg hatching success up to the third mating, and it had costs in terms of reduced fecundity, reduced egg hatching success after the third mating, and lower offspring size. The level of polyandry seems to vary with the female optimum, regulated by a satiation-dependent resistance to mating, potentially leaving satiated females in lifelong virginity.

The extent and costs of reproductive interference among four species of true bug

AbstractReproductive interference arises when individuals of one species engage in reproductive activities with individuals of another, leading to fitness costs in one or both species. Reproductive interference (RI) therefore has two components. First, there must be mis‐directed mating interactions. Second, there must be costs associated with these mis‐directed interactions. Here we consider RI between four species of true bug in the family Lygaeidae, focusing in particular on the fitness consequences to Lygaeus equestris. The species we consider vary in their relationships with each other, including species in the same or different genus, and with or without natural overlap in their geographic ranges. First we show that inter‐specific mating interactions, although not a certain outcome, are common enough to perhaps influence mating behaviour in these species (arising in up to 10 % of inter‐specific pairings). Second, we show that reproductive interference can seriously reduce female fitness in L. equestris. Importantly, different species impose different costs of RI on L. equestris, with interactions with male Spilostethus pandurus inflicting fitness costs of similar magnitude to the costs of mating with con‐specifics. On the other hand, mating interactions with male Oncopeltus fasciatus appear to have no effect on female fitness. In a follow‐up experiment, when we allowed competition amongst just females of S. pandurus and L. equestris, the fitness of the latter was not reduced, arguing more strongly for the role of reproductive interference. However, in our final experiments under mass mating conditions with extended ecological interactions (including scope for competition for resources and cannibalism), the costs of RI were less apparent. Our data therefore suggest that the costs of RI will be context‐specific and may act in concert with, or be swamped by, other ecological effects. We suggest that comparative studies of this sort that both mimic naturally occurring reproductive interference events, and also artificially generate new ones, will be necessary if we are to better understand the ecological and evolutionary significance of reproductive interference.

Receptive females mitigate costs of sexual conflict.

Males typically gain fitness from multiple mating, whereas females often lose fitness from numerous mating, potentially leading to sexual conflict over mating. This conflict is expected to favour the evolution of female resistance to mating. However, females may incur male harassment if they refuse to copulate; thus, greater female resistance may increase costs imposed by males. Here, I show that the evolution of resistance to mating raises fitness disadvantages of interacting with males when mating is harmful in female adzuki bean beetles, Callosobruchus chinensis. Females that were artificially selected for higher and lower remating propensity evolved to accept and resist remating, respectively. Compared with females that evolved to accept remating, females that evolved to resist it suffered higher fitness costs from continuous exposure to males. The costs of a single mating measured by the effect on longevity did not differ among selection line females. This study indicates that receptive rather than resistant females mitigate the fitness loss resulting from sexual conflict, suggesting that even though mating is harmful, females can evolve to accept additional mating.

Do gynogenetic species escape evolving enemies?

Gynogenetic organisms are asexual females of one species that require sperm from males of another species to initiate reproduction (but except in rare instances of ‘paternal leakage’, those sperm do not contribute to the genetic make-up of the gynogens’ offspring). Gynogenetic organisms seem to combine disadvantages of both sexual and asexual reproductive strategies (e.g., mating costs, reduced genetic diversity). We borrowed logic from the Red Queen Hypothesis (RQH) to help explain the persistence of gynogenetic species in nature, which is a paradox. The RQH is the most oft-cited explanation for the maintenance of sex. It states that evolving enemies generate a constantly changing environment, which provides the conditions that make sex advantageous. Under this scenario, asexual organisms cannot evolve fast enough to ‘keep up’ with co-evolving parasites and disease causing organisms, and ultimately show reduced fitness compared to sexual individuals. The RQH tends to view asexuality generally, ignoring important nuance in nature like gynogenetic species in mixed assemblages with closely related sexual species. We outline tests of the argument that sperm dependency prevents asexual gynogens from outcompeting sexuals in mixed species assemblages and that this further allows gynogens to escape evolving enemies.

Female and male fitness consequences of clonal growth in a dwarf bamboo population with a high degree of clonal intermingling.

Although many studies have reported that clonal growth interferes with sexual reproduction as a result of geitonogamous self-pollination and inbreeding depression, the mating costs of clonal growth are expected to be reduced when genets are spatially intermingled with others. This study examined how clonal growth affects both female and male reproductive success by studying a population of a mass-flowering plant, Sasa veitchii var. hirsuta, with a high degree of clonal intermingling. In a 10 × 10 m plot, genets were discriminated based on the multilocus genotypes of 11 nuclear microsatellite loci. The relationships between genet size and the components of reproductive success were then investigated. Male siring success and female and male selfing rates were assessed using paternity analysis. A total of 111 genets were spatially well intermingled with others. In contrast to previous studies with species forming distinct monoclonal patches, seed production linearly increased with genet size. While male siring success was a decelerating function of genet size, selfing rates were relatively low and not related to genet size. The results, in conjunction with previous studies, emphasize the role of the spatial arrangement of genets on both the quantity and quality of offpsring, and suggest that an intermingled distribution of genets can reduce the mating costs of clonal growth and enhance overall fitness, particularly female fitness.

Reduced sexual functionality of PI‐Wolbachia‐infected females of Tetrastichus coeruleus

AbstractWolbachia are endosymbiotic bacteria known to manipulate the reproduction of their hosts by, for example, inducing parthenogenesis. In most cases of Wolbachia‐induced parthenogenesis, the infection is fixed and the entire host population consists of females. In the absence of males and sexual reproduction, genes involved in sexual reproduction are not actively maintained by selection. Accumulation of neutral mutations or selection against maintenance of sexual traits may lead to their loss or deterioration. In addition, females may lose the ability to reproduce sexually due to ‘functional virginity mutations’ that may spread concomitantly with the Wolbachia infection through a population. The parasitoid wasp Tetrastichus coeruleus (Nees) (Hymenoptera: Eulophidae) forms an ideal model to study the decay of sexual functionality, because it has both Wolbachia‐infected, parthenogenetic populations and uninfected, sexual populations. We compared several components of sexual functionality of arrhenotokous (sexual) and thelytokous (parthenogenetic) T. coeruleus females. First, we tested whether arrhenotokous and thelytokous females were equally attractive and receptive to males. Second, we examined whether mating is costly to females by measuring the life span of mated and virgin females. Last, we studied the morphology of the spermathecae of arrhenotokous and thelytokous females. Mated females had shorter life spans than virgin females, showing that mating carried a fitness cost. Two sexual traits of thelytokous females have degraded compared to arrhenotokous females. Arrhenotokous and thelytokous females were equally attractive to males, but thelytokous females were unreceptive to males. Furthermore, there was a clear difference in spermathecal morphology between arrhenotokous and thelytokous females. Our data do not allow distinction between the various potential causes of such degradation. Although the longevity cost of mating may indicate selection against the maintenance of costly sexual traits, accumulation of neutral mutations, functional virginity mutations, manipulation by Wolbachia, and/or the genetic distance between the two populations may all have contributed to the decay of sexual traits in thelytokous females.

Environmental, social, morphological, and behavioral constraints on opportunistic multiple paternity

Multiple mating and multiple paternity in polytocous species have been mostly studied from an adaptive (i.e., cost–benefit) perspective. Disease, time, energy, and the risk of injuries are well-known costs of multiple mating, yet from both male and female perspectives, a number of genetic and non-genetic benefits have also been identified. The effects of environmental conditions and individual-specific behavior, however, are much less well understood. Using a long-term study on yellow-bellied marmots (Marmota flaviventris), we evaluated the impacts of environmental variation, social structure, female body mass, and female docility (a personality trait) on the occurrence of multiple paternity. Multiple paternity was influenced by environmental constraints, social constraints, a female’s personality, and her body mass at emergence from hibernation. Personality and mass effects were detected only when environmental or social conditions were favorable. Our results suggest that multiple paternity is mainly limited by the opportunity to have access to multiple mates and is influenced by costs or mate choice because heavier females were more likely to have litters with multiple sires than smaller ones. Future studies in other species might benefit from considering environmental constraints when studying multiple paternity.

The rise of monogamy

Why has polygyny, marriage of a man to multiple women, common in most societies throughout history, almost disappeared in modern industrialized countries? Do women play a role in its disappearance? A simple theoretical model suggests that at the later stage of the transition from polygyny to monogamy, the spread of human capital and the increase of labor income have led to the rise of monogamy. A general equilibrium model of the marriage market illustrates that the spread of human capital results in an increase in women’s income opportunities and lowers the importance of bequests in determining their sons’ incomes. Both effects improve women’s outside option, mating monogamously, and decrease the marginal benefit of the economic advantages provided by polygynous unions. This, in turn, reduces polygyny by increasing the cost of polygynous mating for men. When the human capital level is sufficiently high, men find it optimal to marry monogamously instead of bearing the high cost of polygynous mating.